Abstract
BackgroundThe cosmopolitan freshwater snail Physa acuta has recently found widespread use as a model organism for the study of mating systems and reproductive allocation. Mitochondrial DNA phylogenies suggest that Physa carolinae, recently described from the American southeast, is a sister species of P. acuta. The divergence of the acuta/carolinae ancestor from the more widespread P. pomilia appears to be somewhat older, and the split between a hypothetical acuta/carolinae/pomilia ancestor and P. gyrina appears older still.ResultsHere we report the results of no-choice mating experiments yielding no evidence of hybridization between gyrina and any of four other populations (pomilia, carolinae, Philadelphia acuta, or Charleston acuta), nor between pomilia and carolinae. Crosses between pomilia and both acuta populations yielded sterile F1 progeny with reduced viability, while crosses between carolinae and both acuta populations yielded sterile F1 hybrids of normal viability. A set of mate-choice tests also revealed significant sexual isolation between gyrina and all four of our other Physa populations, between pomilia and carolinae, and between pomilia and Charleston acuta, but not between pomilia and the acuta population from Philadelphia, nor between carolinae and either acuta population. These observations are consistent with the origin of hybrid sterility prior to hybrid inviability, and a hypothesis that speciation between pomilia and acuta may have been reinforced by selection for prezygotic reproductive isolation in sympatry.ConclusionsWe propose a two-factor model for the evolution of postzygotic reproductive incompatibility in this set of five Physa populations consistent with the Dobzhansky-Muller model of speciation, and a second two-factor model for the evolution of sexual incompatibility. Under these models, species trees may be said to correspond with gene trees in American populations of the freshwater snail, Physa.
Highlights
The cosmopolitan freshwater snail Physa acuta has recently found widespread use as a model organism for the study of mating systems and reproductive allocation
The purpose of the work we present here is to examine the origin of reproductive isolation in a simultaneous hermaphrodite from a phylogenetic perspective
Sexual isolation As has previously been documented [45,58,59], our approach of rearing snails to adulthood in isolation before initiating mate-choice tests seemed to yield many animals eager to copulate in the male role, while rejective in the female role
Summary
The cosmopolitan freshwater snail Physa acuta has recently found widespread use as a model organism for the study of mating systems and reproductive allocation. Mitochondrial DNA phylogenies suggest that Physa carolinae, recently described from the American southeast, is a sister species of P. acuta. The mechanisms of reproductive isolation have been elucidated only in the marine prosobranch snail Littorina [9,10], opisthobranch sea slugs [11], certain terrestrial (stylommatophoran) pulmonates [12,13], and in the freshwater (basommatophoran) pulmonates that will be the focus of the present work. With regard to postzygotic reproductive isolation, experiments with F2 backcrosses among Drosophila species have consistently demonstrated that hybrid sterility is attributable to genes on every arm of every chromosome [15]. Thirteen loci in seven linkage groups were implicated in the origin of postzygotic isolation speciation among lake whitefish by Rogers and Bernatchez [17]
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